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      Effect of Poor Access to Water and Sanitation As Risk Factors for Soil-Transmitted Helminth Infection: Selectiveness by the Infective Route

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          Abstract

          Background

          Soil-transmitted helminth (STH) infections are a public health problem in resource-limited settings worldwide. Chronic STH infection impairs optimum learning and productivity, contributing to the perpetuation of the poverty-disease cycle. Regular massive drug administration (MDA) is the cardinal recommendation for its control; along with water, sanitation and hygiene (WASH) interventions. The impact of joint WASH interventions on STH infections has been reported; studies on the independent effect of WASH components are needed to contribute with the improvement of current recommendations for the control of STH. The aim of this study is to assess the association of lacking access to water and sanitation with STH infections, taking into account the differences in route of infection among species and the availability of adequate water and sanitation at home.

          Methods and Findings

          Cross-sectional study, conducted in Salta province, Argentina. During a deworming program that enrolled 6957 individuals; 771 were randomly selected for stool/serum sampling for parasitological and serological diagnosis of STH. Bivariate stratified analysis was performed to explore significant correlations between risk factors and STH infections grouped by mechanism of entry as skin-penetrators (hookworms and Strongyloides stercoralis) vs. orally-ingested ( Ascaris lumbricoides and Trichuris trichiura). After controlling for potential confounders, unimproved sanitation was significantly associated with increased odds of infection of skin-penetrators (adjusted odds ratio [aOR] = 3.9; 95% CI: 2.6–5.9). Unimproved drinking water was significantly associated with increased odds of infection of orally-ingested (aOR = 2.2; 95% CI: 1.3–3.7).

          Conclusions

          Lack of safe water and proper sanitation pose a risk of STH infections that is distinct according to the route of entry to the human host used by each of the STH species. Interventions aimed to improve water and sanitation access should be highlighted in the recommendations for the control of STH.

          Author Summary

          Soil-transmitted helminths (STH) are a group of parasitic human infections of great public health relevance due to their high prevalence and potentially severe morbidity in case of heavy infection intensity, especially in poor settings. Common species of STH include Ascaris lumbricoides, Trichuris trichiura, Hookworm ( Ancylostoma duodenale and Necator americanus) and Strongyloides stercoralis. Their life cycle includes an obligatory passage on soil, where they mature becoming capable of transmitting the infection to a new host. Two infective routes can be distinguished according to the species, oral ingestion of eggs versus skin penetration of larvae from fecally contaminated soil. Inadequate sanitation and unsafe water supply were described as risk factors for STH infections; however more data on this relationship is needed. The main strategy for STH control is the regular deworming, through mass drug administration. Interventions on water, sanitation and hygiene (WASH) and health education are also important to sustain the benefits of anthelmintic therapy. The present study reports an association between poor sanitation and water access and STH infections selective to the parasite route of entry. This finding could contribute to the design of specific and rational recommendations to reduce soil-transmitted helminths transmission.

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          Most cited references 26

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          Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm.

          The three main soil-transmitted helminth infections, ascariasis, trichuriasis, and hookworm, are common clinical disorders in man. The gastrointestinal tract of a child living in poverty in a less developed country is likely to be parasitised with at least one, and in many cases all three soil-transmitted helminths, with resultant impairments in physical, intellectual, and cognitive development. The benzimidazole anthelmintics, mebendazole and albendazole, are commonly used to remove these infections. The use of these drugs is not limited to treatment of symptomatic soil-transmitted helminth infections, but also for large-scale prevention of morbidity in children living in endemic areas. As a result of data showing improvements in child health and education after deworming, and the burden of disease attributed to soil-transmitted helminths, the worldwide community is awakening to the importance of these infections. Concerns about the sustainability of periodic deworming with benzimidazole anthelmintics and the emergence of resistance have prompted efforts to develop and test new control tools.
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            Control of neglected tropical diseases.

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              Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis.

              More than a quarter of the human population is likely infected with soil-transmitted helminths (Ascaris lumbricoides, hookworm, and Trichuris trichiura) in highly endemic areas. Preventive chemotherapy is the mainstay of control, but only 4 drugs are available: albendazole, mebendazole, levamisole, and pyrantel pamoate. To assess the efficacy of single-dose oral albendazole, mebendazole, levamisole, and pyrantel pamoate against A lumbricoides, hookworm, and T trichiura infections. A systematic search of PubMed, ISI Web of Science, ScienceDirect, the World Health Organization library database, and the Cochrane Central Register of Controlled Trials (1960 to August 2007). From 168 studies, 20 randomized controlled trials were included. Information on study year and country, sample size, age of study population, mean infection intensity before treatment, diagnostic method used, time between evaluations before and after treatment, cure rate (the percentage of individuals who became helminth egg negative following treatment with an anthelminthic drug), egg reduction rate, adverse events, and trial quality was extracted. Relative risk, including a 95% confidence interval (CI), was used to measure the effect of the drugs on the risk of infection prevalence with a random-effects model. Single-dose oral albendazole, mebendazole, and pyrantel pamoate for infection with A lumbricoides resulted in cure rates of 88% (95% CI, 79%-93%; 557 patients), 95% (95% CI, 91%-97%; 309 patients), and 88% (95% CI, 79%-93%; 131 patients), respectively. Cure rates for infection with T trichiura following treatment with single-dose oral albendazole and mebendazole were 28% (95% CI, 13%-39%; 735 patients) and 36% (95% CI, 16%-51%; 685 patients), respectively. The efficacy of single-dose oral albendazole, mebendazole, and pyrantel pamoate against hookworm infections was 72% (95% CI, 59%-81%; 742 patients), 15% (95% CI, 1%-27%; 853 patients), and 31% (95% CI, 19%-42%; 152 patients), respectively. No pooled relative risks could be calculated for pyrantel pamoate against T trichiura and levamisole for any of the parasites investigated. Single-dose oral albendazole, mebendazole, and pyrantel pamoate show high cure rates against A lumbricoides. For hookworm infection, albendazole was more efficacious than mebendazole and pyrantel pamoate. Treatment of T trichiura with single oral doses of current anthelminthics is unsatisfactory. New anthelminthics are urgently needed.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                30 September 2015
                September 2015
                : 9
                : 9
                Affiliations
                [1 ]Instituto de Investigaciones en Enfermedades Tropicales (IIET), Universidad Nacional de Salta–Sede Regional Orán, San Ramón de la Nueva Orán, Salta, Argentina
                [2 ]Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
                [3 ]Dirección Nacional de Prevención de Enfermedades y Riesgos, Ministerio de Salud de la Nación, Buenos Aires, Argentina
                [4 ]Fundación Mundo Sano, Buenos Aires, Argentina
                [5 ]Hospital Juan Domingo Perón, Tartagal, Salta, Argentina
                Swiss Tropical and Public Health Institute, SWITZERLAND
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AE DB MJ SPC VH SC ROC PAV NC GP AJK. Performed the experiments: AE MJ SPC VH SC ROC PAV NC AJK. Analyzed the data: AE DB MJ AJK. Contributed reagents/materials/analysis tools: AE DB MJ SPC VH SC ROC PAV NC GP AJK. Wrote the paper: AE DB MJ SPC VH SC ROC PAV NC GP AJK.

                Article
                PNTD-D-15-01082
                10.1371/journal.pntd.0004111
                4589369
                26421865

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

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                Figures: 3, Tables: 3, Pages: 14
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                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
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                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology

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